Mnemonic introspection in macaques is dependent on superior dorsolateral prefrontal cortex but not orbitofrontal cortex

Abstract

The human PFC has been associated more with meta-perceptual as opposed to meta-memory decisions from correlational neuroimaging investigations. Recently, metacognitive abilities have also been shown to be causally dependent upon anterior and dorsal PFC in nonhuman primate lesion studies.Two studies, using postdecision wagering paradigmsandreversible inactivation, challenged this meta-perceptual versus meta-memory notion and showed that dorsal and anterior prefrontal areas are associated with metamemory for experienced objects and awareness of ignorance, respectively. Causal investigations are important but scarce; nothing is known, for example, about the causal contributions of prefrontal subregions to spatial metamemory. Here, we investigated the effects of dorsal versus ventral PFC lesions on two-alternative forced-choicespatialdiscriminationtasks inmalemacaquemonkeys.Importantly,wewererigorousinapproachandappliedthreeindependent but complementary indices used to quantify individual animals’ metacognitive ability (“Type II sensitivity”) by two variants of meta-d‘/d‘ and phi coefficient (φ). Our results were consistent across indices: while neither lesions to superior dorsolateral PFC nor orbitofrontal cortex impaired spatial recognition performance, onlymonkeyswith superior dorsolateralPFClesions were impaired in meta-accuracy. Together with the observation that the same orbitofrontal cortex lesioned monkeys were impaired in updating rule value in a Wisconsin Card Sorting Test analog, we therefore document a functional double-dissociation between these two PFC regions. Our study presents important causal evidence thatotherdimensions,namely,domain-specificprocessing(e.g., spatialvsnonspatialmetamemory),alsoneedconsiderationsinunderstanding the functional specialization in the neural underpinnings of introspection.